Biology subjects

de Busserolles, F.

Publications and source records attributed to de Busserolles, F..

9 recordsLinked to original sources

bioRxiv2026

Rapid evolution of cone identity and retinal topography in deep-water crater lake cichlids

Deep-water habitats have been colonized repeatedly by fishes, driving the evolution of visual systems under extremely low-light conditions. Here, we investigated visual adaptation in cichlids from the Barombi Mbo crater lake by comparing shallow- and deep-water species using retinal single-cell transcriptomics and analyses of retinal specializations. The shallow-water species Pungu maclareni expressed a broader repertoire of visual opsins across distinct populations of short- (SWS), medium- (RH2), and long-wavelength-sensitive (LWS) cone photoreceptors. In contrast, the deep-water species Myaka myaka lacked a distinct LWS cone population and instead relied predominantly on RH2A/{beta}-expressing, green-sensitive photoreceptors. To assess whether these deep-water RH2 cones corresponded to canonical RH2 or LWS programmes, we compared conserved photoreceptor markers. Deep-water RH2 cones retained elements of both RH2- and LWS-associated transcriptional programmes, revealing a mixed profile lacking a clear canonical cone-type signature. LWS-associated transcriptional regulators also differed between species, with tbx2a absent from M. myaka cones, consistent with the loss of LWS opsin expression, whereas thrb persisted in M. myaka RH2 cones. We further examined retinal specialization across eight species from the radiation and found that retinal topography also differed in photoreceptor distributions and ganglion cell-based acuity centers in association with habitat depth but also with trophic ecology of the species. Together, our findings show that visual adaptation in a young adaptive radiation involves coordinated changes in visual opsin expression, cone-associated transcriptional programmes, and retinal organization, highlighting how sensory systems can quickly evolve through changes at multiple biological levels in response to ecological conditions.

evolutionary biology↗

bioRxiv2024

Deep-sea fish reveal alternative pathway for vertebrate visual development

Vertebrate vision is accomplished by two phenotypically distinct types of photoreceptors in the retina: the saturation-resistant cones for the detection of bright light and the highly sensitive rods for dim light conditions [1]. The current dogma is that, during development, all vertebrates initially feature a cone-dominated retina, and rods are added later [2, 3]. By studying the ontogeny of vision in three species of deep-sea fishes, we show that their larvae express cone-specific genes in photoreceptors with rod-like morphologies. Through development, these fishes either retain this rod-like cone retina (Maurolicus mucronatus) or switch to a retina with true rod photoreceptors with expression of rod-specific genes and transcription factors (Vinciguerria mabahiss and Benthosema pterotum). In contrast to the larvae of most marine fishes, which inhabit the bright upper layer of the open ocean, the larvae of deep-sea fishes occur deeper, exposing them to a dimmer light environment [4-7]. Spectral maxima predictions from molecular dynamics simulations and environmental light estimations suggest that using transmuted photoreceptors that combine the characteristics of both cones and rods maximises visual performance in these dimmer light conditions. Our findings provide molecular, morphological, and functional evidence for the evolution of an alternative developmental pathway for vertebrate vision.

evolutionary biology↗

bioRxiv2022

Multiple rod layers increase the speed and sensitivity of vision in nocturnal reef fishes

Multibank retinas have rod photoreceptors stacked into multiple layers. They are found in many species of fish that inhabit dim environments and are one of the most common visual adaptations in the deep-sea. Despite its prevalence, the function of multibank retinas remained unknown. Two predominant theories, neither of which has been tested, have emerged: 1) they enhance sensitivity in dim light, and 2) they allow colour vision in dim light. To investigate the sensitivity hypothesis, we performed electrophysiological recordings and compared the rod pigments of three species of nocturnal reef fishes, two with a multibank retina (Neoniphon sammara and Myripristis violacea) and a control species with a single rod bank (Ostorhinchus compressus). Results indicated that nocturnal reef fishes with a multibank retina have higher temporal resolution of vision, as indicated by electrophysiology, and that their rhodopsin proteins likely also have faster retinal release kinetics, as suggested by amino acid substitutions. Electrophysiology also showed that the multibank retina conferred greater sensitivity to both dim and bright intensities than a single rod bank and this occurred at times when rod-derived signals usually dominate the visual response. This study provides the first functional evidence for enhanced dim-light sensitivity using a multibank retina while also suggesting novel roles for the adaptation in enhancing bright-light sensitivity and the speed of vision. SignificanceMost vertebrates have one layer of the dim-light active rod photoreceptors; however, some species have multiple layers, known as a multibank retina. We used electrophysiology on nocturnal reef fishes with and without multibank retinas to evaluate the sensory advantage of having multiple rod layers. We show that fish with multibank retinas have both faster vision and enhanced sensitivity to bright and dim light intensities. Thus, we resolve for the first time the function of multibank retinas - one of the most common visual adaptations in the deep sea. Our findings highlight an unconventional vertebrate visual system as well as the visual capabilities of fishes from the most vast (deep sea) and vibrant (reefs) ecosystems on the planet.

zoology↗

bioRxiv2022

Developing and adult reef fish show rapid, reversible light-induced plasticity in their visual system

The visual capabilities of fish are optimised for their ecology and light environment over evolutionary time. Similarly, fish vision can adapt to regular changes in light conditions within their lifetime, e.g., ontogenetic or seasonal variation. However, we do not fully understand how vision responds to irregular short-term changes in the light environment, e.g., algal blooms and light pollution. In this study, we investigated the effect of short-term exposure to unnatural light conditions on opsin gene expression and retinal cell densities in larval and adult diurnal reef fish (convict surgeonfish; Acanthurus triostegus). Results revealed phenotypic plasticity in the retina across ontogeny, particularly in the larvae. The most substantial differences at both molecular and cellular levels were found under constant dim light, while constant bright light or simulated artificial light at night had a lesser effect. Under dim light, larvae and adults increased expression of the cone opsin genes, sws2a, rh2c and lws, within a few days and larvae also decreased densities of cones, inner nuclear layer cells and ganglion cells. These changes likely enhanced vision under the altered light conditions. Thus, our study suggests that plasticity mainly comes into play when conditions are extremely different to the species natural light environment, i.e., a diurnal fish in constant night. Finally, in a rescue experiment on adults, shifts in opsin expression were reverted within 24 hours. Overall, our study showed rapid, reversible light-induced changes in the retina of A. triostegus, demonstrating phenotypic plasticity in the visual system of a reef fish throughout life.

developmental biology↗

bioRxiv2022

Development of dim-light vision in the nocturnal coral reef fish family, Holocentridae

Developmental changes to the visual systems of animals are often associated with ecological shifts. Reef fishes experience a change in habitat between larval life in the shallow open ocean to juvenile and adult life on the reef. Some species also change their lifestyle over this period and become largely nocturnal. While these ecological transitions are well documented, little is known about the ontogeny of nocturnal reef fish vision. Here, we used histology and transcriptomics to investigate visual development in 12 representative species from both subfamilies, Holocentrinae (squirrelfishes) and Myripristinae (soldierfishes), in the nocturnal coral reef fish family, Holocentridae. Results revealed that the visual systems of holocentrids are initially well-adapted to photopic conditions with pre-settlement larvae having high cone densities, high cone opsin gene expression, a broad cone opsin gene repertoire (8 genes) and a multibank retina (i.e., stacked layers of rods) comprising up to two rod banks. At reef settlement, holocentrids started to invest more in their scotopic visual system and upregulated genes involved in cell differentiation/proliferation. By adulthood, they had well-developed scotopic vision with a rod-dominated multibank retina comprising 5-17 rod banks, increased summation of rods onto ganglion cells, high rod opsin gene expression, reduced cone opsin gene expression and repertoire (1-4 genes) and upregulated phototransduction genes. Finally, although the two subfamilies shared similar ecologies across development, their visual systems diverged after settlement, with Myripristinae investing more in scotopic vision than Holocentrinae. Hence, both ecology and phylogeny likely determine the development of the holocentrid visual system. Summary statementCoral reef fishes in the family Holocentridae remodel their retina at the cellular and molecular levels to adapt to a nocturnal lifestyle during development.

developmental biology↗

bioRxiv2020

The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina

The visual systems of teleost fishes usually match their habitats and lifestyles. Since coral reefs are bright and colourful environments, the visual systems of their diurnal inhabitants have been more extensively studied than those of nocturnal species. In order to fill this knowledge gap, we conducted a detailed investigation of the visual systems of the coral reef fish family Holocentridae (squirrelfish and soldierfish). In addition to their nocturnality, this family is particularly interesting for dim-light vision studies due to its ecological and evolutionary connection to deeper habitats. Results showed that the visual system of holocentrids is well adapted to their nocturnal lifestyle with a rod-dominated retina. Surprisingly, rods in all species were arranged into 6-17 well-defined banks, a feature most commonly found in deep-sea fishes, that may increase the light sensitivity of the eye and/or allow colour discrimination in dim-light. Holocentrids also have the potential for dichromatic colour vision during the day with the presence of at least two spectrally different cone types: single cones expressing the blue-sensitive SWS2A gene, and double cones expressing one or two green-sensitive RH2 genes. Some differences were observed between the two subfamilies, with Holocentrinae having a slightly more developed photopic visual system than Myripristinae. Moreover, retinal topography of both ganglion cells and cone photoreceptors showed specific patterns for each cell type, likely highlighting different visual demands at different times of the day, such as feeding. Overall, their well-developed scotopic visual systems and the ease of catching and maintaining holocentrids in aquaria, make them ideal models to investigate teleost dim-light vision and more particularly shed light on the function of multibank retina and its potential for dim-light colour vision.

neuroscience↗

bioRxiv2019

Microhabitat partitioning correlates with opsin geneexpression in coral reef cardinalfishes (Apogonidae)

O_LIVertebrates exhibit diverse visual systems that vary in terms of morphology, number and distribution of spectrally distinct photoreceptor types, visual opsin genes and gene expression levels.\nC_LIO_LIIn fish, such adaptations are driven by two main factors: differences in the light environment and behavioural tasks, including foraging, predator avoidance and mate selection. Whether visual systems also adapt to small-scale spectral differences in light, between microhabitats, is less clear.\nC_LIO_LIWe suggest that differences in microhabitat use by cardinalfishes (Apogonidae) on coral reefs drive morphological and molecular adaptations in their visual systems. To test this, we investigated diurnal microhabitat use in 17 cardinalfish species and assessed whether this correlated with differences in visual opsin gene expression and eye morphology.\nC_LIO_LIWe found that cardinalfishes display six types of partitioning behaviours during the day, ranging from specialists found exclusively in the water column to species that are always hidden inside the reef matrix.\nC_LIO_LIUsing data on visual opsin gene expression previously characterized in this family, it was discovered that species in exposed habitats had increased expression of the short-wavelength sensitive violet opsin (SWS2B) and decreased expression of the dim-light active rod opsin (RH1). Species of intermediate exposure, on the other hand, expressed opsins that are mostly sensitive to the blue-green central part of the light spectrum (SWS2As and RH2s), while fishes entirely hidden in the reef substrate had an increased expression of the long-wavelength sensitive red opsin (LWS).\nC_LIO_LIWe found that eye size relative to body size significantly differed between cardinalfish species, and relative eye size decreased with an increase in habitat exposure.\nC_LIO_LIRetinal topography did not show co-adaptation with microhabitat use, but instead with feeding mode.\nC_LIO_LIWe suggest that, although most cardinalfishes are nocturnal foragers, their visual systems are also adapted to both the light intensity and the light spectrum of their preferred diurnal microhabitat.\nC_LI

ecology↗

bioRxiv2019

Neoteny in visual system development of the spotted unicornfish, Naso brevirostris (Acanthuridae)

Ontogenetic changes of the visual system are often correlated to shifts in habitat and feeding behaviour of animals. Coral reef fishes begin their lives in the pelagic zone and then migrate to the reef. This transition of habitat frequently involves a change in diet and light environment as well as major morphological modifications. The spotted unicornfish, Naso brevirostris, is known to shift diet from zooplankton to algae and back to zooplankton when transitioning from larval to juvenile and then to adult stages. Concurrently, N. brevirostris also moves from an open pelagic to a coral-associated habitat before migrating up in the water column when reaching adulthood. Using retinal mapping techniques, we discovered that the distribution and density of ganglion and photoreceptor cells in N. brevirostris do not change with the habitat or the feeding habits of each developmental stage. Instead, fishes showed a neotenic development with a slight change from larval to juvenile stages and not many modifications thereafter. Visual gene expression based on RNA sequencing mirrored this pattern; independent of stage, fishes mainly expressed three cone opsin genes (SWS2B, RH2B, RH2A), with a quantitative difference in the expression of the green opsin genes (RH2A and RH2B) when transitioning from larvae to juveniles. Hence, contrary to the ontogenetic changes found in many animals, the visual system is fixed early on in N. brevirostris development calling for a thorough analysis of visual system development of the reef fish community.

evolutionary biology↗

bioRxiv2018

Vision using multiple distinct rod opsins in deep-sea fishes

Vertebrate vision is accomplished through a set of light-sensitive photopigments, which are located in the photoreceptors of the retina and consist of a visual opsin protein bound to a chromophore. In dim-light, vertebrates generally rely upon a single rod opsin (RH1) for obtaining visual information. By inspecting 101 fish genomes, we found that three deep-sea teleost lineages have independently expanded their RH1 gene repertoires. Amongst these, the silver spinyfin (Diretmus argenteus Johnson 1863) stands out as having the highest number of visual opsins known for animals to date (2 cone and 38 rod opsins). Spinyfins simultaneously express up to 14 RH1s encoding for photopigments with different peak spectral sensitivities ({lambda}max=448-513 nm) that cover the range of the residual daylight, as well as the bioluminescence spectrum present in the deep-sea. Our findings present novel molecular and functional evidence for the recurrent evolution of multiple rod opsin-based vision in vertebrates.\n\nSHORT ABSTRACTContrary to the single rod opsin used by most vertebrates, some fishes use multiple rod opsins for vision in the dimly lit deep-sea.

evolutionary biology↗